Alien freshwater fish parasites from South Africa

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Class: Phyllopharyngea. Order: Chlamydodontida. Family: Chilodonellidae. Chilodonella hexasticha. Co- invasive. Coptodon rendalli Lebowa Fisheries Station.
International Journal for Parasitology: Parasites and Wildlife xxx (2017) 1e16

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International Journal for Parasitology: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw

Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward Nico J. Smit a, *, Wynand Malherbe a, Kerry A. Hadfield a, b a b

Water Research Group, Unit for Environmental Sciences and Management, North-West University, 11 Hoffman St, Potchefstroom, 2520, South Africa Department of Zoology and Entomology, University of the Free State, Bloemfontein, South Africa

a r t i c l e i n f o

a b s t r a c t

Article history: Received 3 March 2017 Received in revised form 30 May 2017 Accepted 1 June 2017

The global translocation and introduction of freshwater fish into non-native regions has created the perfect opportunity for the co-introduction of their parasites. In a recent review on non-native freshwater fish introductions in South Africa, 55 fishes were reported as introduced into novel environments in South Africa, with 27 alien and 28 extralimital. However, the parasites potentially co-introduced by these non-native fishes have received much less attention from researchers than the hosts themselves. Thus far, the only attempts at summarising our knowledge on the diversity of introduced freshwater fish parasites in this region dates back to the 1980s when only four parasite species were considered to be alien, with a further eight species as doubtful. Over the last thirty years, more records have been added and this paper aims to provide an up-to-date review of our knowledge on the diversity, distribution, status (co-invasive or co-introduced) and the direction for future studies on introduced freshwater fish parasites in South Africa. Here we consider seven species (four ciliates, and one cestode, copepod and branchiuran respectively) as confirmed co-invaders, and 16 species (one flagelate, four ciliates, one cestode and ten monogeneans) as co-introduced. In addition, six species (three ciliates, two monogeneans and one copepod) previously recorded as invasive are deemed to be of uncertain status, and one ciliate is removed from the list of known invasive parasites from this region. It is further proposed that future research should focus on extralimital co-introductions, especially in the Eastern and Western Cape regions of South Africa where more than half of the fishes present are introduced species. It is also recommended that all new records of introduced parasites and new distribution records of known invasive parasites should include the deposition of voucher specimens in museums and, as far as possible, include molecular confirmation of its identification. © 2017 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords: Alien invasive Fish parasites Co-introduction Co-invasive

Contents 1. 2.

3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Confirmed co-invasive freshwater fish parasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Phylum Ciliophora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. Ichthyophthirius multifiliis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.2. Apiosoma piscicola . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.3. Chilodonella hexasticha . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.4. Chilodonella piscicola (syn. C. cyprini) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Phylum Platyhelminthes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1. Schyzocotyle (Bothriocephalus) acheilognathi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Phylum Arthropoda . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1. Lernaea cyprinacea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2. Argulus japonicus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Confirmed co-introduced freshwater fish parasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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* Corresponding author. E-mail address: [email protected] (N.J. Smit). http://dx.doi.org/10.1016/j.ijppaw.2017.06.001 2213-2244/© 2017 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Smit, N.J., et al., Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward, International Journal for Parasitology: Parasites and Wildlife (2017), http://dx.doi.org/10.1016/j.ijppaw.2017.06.001

2

N.J. Smit et al. / International Journal for Parasitology: Parasites and Wildlife xxx (2017) 1e16

3.1.

4.

5.

6.

Phylum Euglenozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1. Ichthyobodo necator . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Phylum Ciliophora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1. Trichodina acuta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2. Trichodina mutabilis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.3. Trichodina reticulata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.4. Trichodina uniforma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Phylum Platyhelminthes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1. Atractolytocestus huronensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2. Acolpenteron ureteroecetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.3. Dactylogyrus extensus, Dactylogyrus minutus and Dactylogyrus lamellatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.4. Gyrodactylus kherulensis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.5. Ancyrocephalid monogeneans of largemouth bass, Micropterus salmoides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Parasites of uncertain invasive status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Phylum Ciliophora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.1. Apiosoma nasalis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1.2. Trichodinella epizootica and Trichodina nigra . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Phylum Platyhelminthes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1. Gyrodactylus kobayashii . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2. Pseudodactylogyrus anguillae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Phylum Arthropoda . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.1. Achtheres pimelodi (syn. Achtheres micropteri) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Species previously reported as invasive but hereby removed from the list . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Phylum Ciliophora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.1. Trichodina pediculus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions and future direction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Worldwide, the translocation and subsequent introduction of freshwater fish into non-native regions is known to cause an effect on the native biota. However, a secondary ecological and economical risk is also created but often disregarded. This risk is the co-introduction of the alien invasive fish parasites. Potential impacts of parasites due to host switching from introduced to a native host have been well documented (Adlard et al., 2015). Probably the best studied example is the introduction of the swim bladder nematode, Anguillicoloides crassus (Kuwahara, Niimi and Itagaki, 1974), into Europe and subsequent impact on wild European eels, Anguilla anguilla (Linnaeus, 1758). In a recent review on non-native freshwater fish introductions in South Africa, Ellender and Weyl (2014) listed a total of 55 fishes that have been introduced into novel environments in South Africa, with 27 alien and 28 extralimital (native to South Africa that have been translocated into areas where they did not naturally occur) introductions. These authors also emphasised that the introduction of associated parasites is a serious threat to native fish communities in South Africa. To date, the only available checklist for freshwater fish parasites from southern Africa is the work done in the 1980s by Van As and Basson (1984). Ninety-five species of parasites were listed from 52 hosts and included 13 presumed alien parasites, although the authors did not specifically identify them as alien. Most of these (10) were protozoans with the remaining three being a cestode, a copepod, and a branchiuran respectively (see Table 1). Of the 52 hosts listed, only four were invasive fishes infected with nine of the alien parasites recorded from southern African fishes at that stage. The common carp, Cyprinus carpio Linnaeus, 1758, was clearly responsible for most of the co-introductions and co-invasions into South Africa with seven of the thirteen parasites recorded from this host (Table 2). The first attempt to summarise the extent of aquatic

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introductions into southern Africa was by Bruton and Merron (1985), who compiled a checklist of alien and translocated aquatic animals from this region. In their report, Bruton and Merron (1985) listed 12 fish parasites, including 11 reported by Van As and Basson (1984) with the addition of the copepod Achtheres pimelodi Kroyer, 1863 (syn. Achtheres micropteri Wright, 1882). However, they only regarded four as alien with the status of the remaining eight species considered doubtful; suggesting that further taxonomic research might reveal that they are indigenous. In a book chapter on biological invasions in southern Africa, Bruton and Van As (1986) confirmed the assessment made by Bruton and Merron (1985) without adding additional information. Two years later, De Moor and Bruton (1988) published the first atlas of alien and translocated aquatic animals from southern Africa and only included the four fish parasites considered by Bruton and Merron (1985) as alien. These were the European trichodinid, Trichodina acuta Lom 1961 (ciliate); whitespot, Ichthyophthirius multifiliis Fouquet, 1876 (ciliate); Asian fish tape worm, Schyzocotyle (Bothriocephalus) acheilognathi Yamaguti, 1934 (cestode); and the Japanese fish louse, Argulus japonicus Thiele, 1900 (branchiuran). The most recent checklist of alien animals of southern Africa is a photo guide book by Picker and Griffiths (2011) that included all freshwater, marine and terrestrial species. These authors included two of the four species reported by De Moor and Bruton (1988) (A. japonicus and S. acheilognathi) and added the gill flukes Gyrodactylus kherulensis Ergens, 1974 and Pseudodactylogyrus anguillae (Yin and Sproston, 1948). In addition to the checklist, atlas, and guides mentioned above, many independent studies on specific aspects of alien freshwater parasites were undertaken during the past four decades, however, not a single publication attempted to provide a concise summary of our knowledge on this important subject. The aim of this review is thus to provide an up-to-date review of our knowledge on alien

Please cite this article in press as: Smit, N.J., et al., Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward, International Journal for Parasitology: Parasites and Wildlife (2017), http://dx.doi.org/10.1016/j.ijppaw.2017.06.001

Table 1 Alien fish parasites found within South Africa indicating their invasion status, as well as recorded hosts, locality records and primary reference. Genus Species

Phylum: Euglenozoa Class: Kinetoplastea Order: Prokinetoplastida Family: Ichthyobodonidae

Ichthyobodo necator Coinvader

Phylum Ciliophora Class: Oligohymenophorea Order: Mobilida Family: Trichodinidae

Trichodina acuta Trichodinella epizootica

Order: Hymenostomatida Family: Ichthyophthiriidae

Order: Sessilida Family: Epistylididae

Status

Host fish

Location - River system

Reference

Cyprinus carpio

Not specified

Todal et al. (2004)

CoOncorhynchus Metsimatsho River introduced mykiss Uncertain Carassius auratus Modder River

Basson and Van As (1993) Basson et al. (1983)

Cyprinus carpio Trichodina mutabilis CoCarassius auratus introduced Trichodina nigra Uncertain Carassius auratus Cyprinus carpio Trichodina CoCarassius auratus reticulata introduced Trichodina uniforma CoCarassius auratus introduced

Modder River Commercial supplier (Cape Town)

Basson et al. (1983) Mouton et al. (2001)

Modder River Modder River Local distributor (Bloemfontein)

Basson et al. (1983) Basson et al. (1983) Basson and Van As (1993)

Komatipoort River (Fish farm)

Van As and Basson (1989)

Ichthyophthirius multifiliis

Keiskamma

Jackson (1978)

Apiosoma nasalis Apiosoma piscicola

Coinvasive

Anguilla mossambica Cyprinus carpio Carassius auratus Enteromius (Barbus) paludinosus Poecilia reticulata Oncorhynchus mykiss Oreochromis mossambicus Salmo trutta

Uncertain Pseudocrenilabrus philander CoCoptodon rendallii invasive Enteromius (Barbus) paludinosus Enteromius (Barbus) trimaculatus Labeo cylindricus Marcusenius macrolepidotus Micropterus dolomieu Oreochromis mossambicus

N.J. Smit et al. / International Journal for Parasitology: Parasites and Wildlife xxx (2017) 1e16

Please cite this article in press as: Smit, N.J., et al., Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward, International Journal for Parasitology: Parasites and Wildlife (2017), http://dx.doi.org/10.1016/j.ijppaw.2017.06.001

Classification

Lowveld Fisheries Research Station; Tompi Seleka; Olifants River Van As et al. (1984); Basson (1982) Commercial suppliers Mouton et al. (2001) Turfloop Dam Basson (1982)

Commercial suppliers Bushmans River Trout Farm; Ingwagwana River; Polela River

Mouton et al. (2001) Bragg (1991)

Lowveld Fisheries Research Station; Sheshego Dam

Van As et al. (1984); Basson (1982)

Bushmans River

Bragg (1991)

Westdene Dam

Viljoen and Van As (1983)

Groot-Letaba River

Viljoen and Van As (1985)

Vaal River

Viljoen and Van As (1985)

Nwanedzi River; Olifants River

Viljoen and Van As (1985)

Mothlapitse River; Nwanedzi River; Olifants River Olifants River

Viljoen and Van As (1985) Viljoen and Van As (1985)

Sabie River

Viljoen and Van As (1985)

Nwanedzi River; Olifants River; Klein Letaba River; Mogalakwena Viljoen and Van As (1985) River; Tompi Seleka and Lowveld Fisheries Stations; Sabie River; Groot-Letaba River; Lepellane River Pseudocrenilabrus Mooi River; Vaal River; Nwanedzi River; Olifants River; Viljoen and Van As (1983, 1985) philander Westdene Dam; Lydenburg Fisheries 3

(continued on next page)

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Classification Class: Phyllopharyngea Order: Chlamydodontida Family: Chilodonellidae

Genus Species

Status

Host fish

Chilodonella hexasticha

Coinvasive

Coptodon rendalli Lebowa Fisheries Station

Chilodonella piscicola (syn. C. cyprini)

Phylum: Platyhelminthes Class: Cestoda Order: Bothriocephalidea Family: Bothriocephalidae

Order: Caryophyllidea Family: Lytocestidae

Schyzocotyle acheilognathi (syn. B. acheilognathi)

Atractolytocestus huronensis

Coinvasive

Coinvasive

Enteromius (Barbus) paludinosus Pseudocrenilabrus philander Oreochromis mossambicus Tilapia sparrmanii Coptodon rendalli

Location - River system

Reference

Basson (1982); Van As and Basson (1984)

Turfloop Dam

Basson (1982); Van As and Basson (1984)

Nwanedzi River; Pietersburg Dam

Van As and Basson (1984)

Olifants River; Pietersburg Dam; Kouga River; Nyl River; Lebowa Paperna and Van As (1983); Basson (1982); Van As and Basson (1984) Fisheries Station; Nwanedzi River Olifants River; Lebowa Fisheries Station Paperna and Van As (1983) University of Johannesburg aquarium; Olifants River Basson (1982); Van As and Basson (1984)

Oreochromis Lowveld Fisheries Research Station mossambicus Pseudocrenilabrus Vaal River (Christiana); Orlando Dam (Klip River in Vaal River) philander Tilapia sparrmanii Lowveld Fisheries Research Station

Van As and Basson (1984)

Cyprinus carpio

Komatipoort - commercial ponds; Olifants River; Vaal River; Mtata River

Boomker et al. (1980); Brandt et al. (1980, 1981); Van As et al. (1981); Schramm (1992)

Enteromius annectens Enteromius argenteus Enteromius bifrenatus Enteromius brevipinnis Enteromius mattozi Enteromius paludinosus Enteromius trimaculatus Labeobarbus maraquensis Labeobarbus aeneus Labeobarbus kimberleyensis

Phongolo River

Current study

Olifants River

Mashego (1982)

Phongolo River

Current study

Marite River (Sabie River)

Schult and Schoonbee (1999)

Olifants River

Mashego (1982)

Olifants River

Mashego (1982)

Mooi River; Olifants River

Van As et al. (1981); Mashego (1982)

Olifants River

Mashego (1982)

Vaal River; Great Fish River

Bertasso and Avenant-Oldewage (2005); Stadtlander et al. (2011)

Vaal River

Brandt et al. (1981); Bertasso and Avenant-Oldewage (2005)

Olifants River; Letaba River; Vaal River; Riet River

Scholz et al. (2015); Current study

CoCyprinus carpio introduced

Basson (1982); Van As and Basson (1984) Van As and Basson (1984)

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Table 1 (continued )

Family: Pseudodactylogyridae Order: Gyrodactylidea Family: Gyrodactylidae

€n Dam; Thomas Baine Nature Reserve Friedrichskro

Truter et al. (2017)

Thomas Baines Nature Reserve

Truter et al. (2017)

€ n Dam Mooi River and Potchefstroom Dam; Friedrichskro

Truter et al. (2017)

Thomas Baines Nature Reserve

Truter et al. (2017)

€n Dam Friedrichskro

Truter et al. (2017)

Jonkershoek inland fish hatchery; Groot-Letaba River (Tzaneen Dam) Jonkershoek inland fish hatchery

Du Plessis (1948); Matla (2012)

Jonkershoek inland fish hatchery

Du Plessis (1948)

Vaal River (Vaal Dam)

Crafford et al. (2014a, b)

Vaal River (Vaal Dam)

Crafford et al. (2014a, b)

Vaal River (Vaal Dam)

Crafford et al. (2014a, b)

Dactylogyrus extensus Dactylogyrus lamellatus Dactylogyrus minutus Pseudodactylogyrus anguillae

Cointroduced CoCyprinus carpio introduced CoCyprinus carpio introduced Uncertain Anguilla mossambica

Gyrodactylus kherulensis

CoCyprinus carpio Kuilsrivier; Durban introduced koi Cyprinus carpio Vaal River (Vaal Dam) Uncertain Carassius auratus Kuilsrivier

Gyrodactylus kobayashii Phylum: Arthropoda Subphylum: Crustacea Class: Maxillopoda Subclass: Copepoda Order: Cyclopoida Family: Lernaeidae

Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus salmoides Micropterus punctulatus Micropterus dolomieu Cyprinus carpio

Lernaea cyprinacea Coinvader

Between Fish and Buffalo Rivers (Eastern Cape); Great Fish River; Christison and Baker (2007); Parker et al. (2011); McHugh et al. (2017) Koonap River; Kei River; Keiskamma River

Achtheres pimelodi

Maseng (2010) Crafford et al. (2014a) Maseng (2010)

Coptodon rendalli Phongolo River

Smit et al. (2016)

Labeo capensis Labeo congoro (syn L. rubropunctatus) Labeo cylindricus Labeo rosae Labeo ruddi Labeo umbratus Labeobarbus marequensis Labeobarbus kimberleyensis Oreochromis mossambicus

Orange River Mogalakwena River; Olifants River;

Robinson and Avenant-Oldewage (1996) Van As and Viljoen (1984); Robinson and Avenant-Oldewage (1996)

Limpopo River Olifants River; Selati River; Olifants River Olifants River Crocodile (West) River; Olifants River; Lowveld Fisheries Station

Van As and Basson (1984) Robinson and Avenant-Oldewage (1996) Robinson and Avenant-Oldewage (1996) Robinson and Avenant-Oldewage (1996) Van As and Basson (1984); Robinson and Avenant-Oldewage (1996)

Vaal River

Robinson and Avenant-Oldewage (1996)

Olifants River; Selati River; Crocodile River (West); Lowveld Fisheries Station; Phongolo River (Nyamiti pan)

Robinson and Avenant-Oldewage (1996); Van As and Viljoen (1984); Van As and Basson (1984); Viljoen (1986); Smit et al. (2016); Welicky et al. (2017) Truter et al. (2016)

Pseudocrenilabrus Harts River (Barberspan) philander Order: Cyclopoida Family: Siphonostomatoida

Du Plessis (1948)

Uncertain Micropterus dolomieu

Not specified

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Class: Monogenea Order: Dactylogyridea Family: Ancyrocephalidae Clavunculus Cobursatus introduced Onchocleidus dispar Cointroduced Onchocleidus Cofurcatus introduced Onchocleidus Coprincipalis introduced Syncleithrium Cofusiformis introduced Family: Dactylogyridae Acolpenteron Coureteroecetes introduced

Barnard (1955); Fryer (1968)

5

(continued on next page)

Avenant-Oldewage (1994); Van As and Basson (1984); AvenantOldewage (2001) Crocodile River (West); Pienaars River; Olifants River

Van As and Basson (1984)

Van As and Basson (1984); Avenant-Oldewage (2001)

Vaal River; Harts River

(1984)

Crocodile River (West) (Hartebeespoort Dam); Pienaars River; Bronkhorstspruit River Lydenburg Fish Hatchery

(1984); Avenant-Oldewage Vaal River; Harts River; Mooi River

Labeobarbus aeneus Labeobarbus kimberleyensis Labeobarbus marequensis Oncorhynchus mykiss Oreochromis mossambicus

(1984); Avenant-Oldewage Olifants River Vaal River; Harts River; Mooi River; Olifants River Labeo rosae Labeo umbratus

(1984); Avenant-Oldewage

Kruger et al. (1983); Van As and Basson (1994) Avenant-Oldewage (1994) Kruger et al. (1983); Van As and Basson (1994); Avenant-Oldewage (2001) Kruger et al. (1983); Van As and Basson (1994) Kruger et al. (1983); Van As and Basson Vaal River; Harts River; Mooi River; Pienaars River

Enteromius mattozi Labeo capensis

Vaal River; Harts River; Pienaars River; Komati River; Olifants River Pienaars River Cyprinus carpio

Clarias gariepinus Vaal River; Olifants River; Pienaars River Coinvasive Argulus japonicus Class: Ichthyostraca Subclass: Branchiura Order: Arguloida Family: Argulidae

Location - River system Host fish Status Genus Species Classification

Table 1 (continued )

Kruger et al. (1983); Van As and Basson (1984); Avenant-Oldewage (1994); Avenant-Oldewage (2001) Kruger et al. (1983); Van As and Basson (1984); Avenant-Oldewage (1994); Avenant-Oldewage (2001) Van As and Basson (1984)

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Reference

6

invasive freshwater fish parasites from South Africa with the specific focus on their status (co-introduced or co-invasive), known distribution, and hosts. Based on our current knowledge and international trends, this paper also aims to provide direction for future studies. 2. Confirmed co-invasive freshwater fish parasites 2.1. Phylum Ciliophora 2.1.1. Ichthyophthirius multifiliis The ciliate I. multifiliis, the causative agent of the disease ichthyophthiriosis, is an important pathogen of freshwater teleosts globally, and accounts for significant economic losses to the aquaculture industry (Matthews, 2005). Similar to many other invasive parasites, I. multifiliis was most likely co-introduced into freshwater ecosystems throughout the world with the introduction of its native cyprinid hosts from Asia (Nigrelli et al., 1976). It was first reported from Africa (Uganda) by Paperna (1972), followed by Jackson (1978) reporting I. multifiliis from the longfin eel, Anguilla mossambica Peters, 1852, collected in the Keiskamma, South Africa (Table 1, Fig. 1A). Other records of I. multifiliis from South Africa include infestations on the introduced C. carpio, Salmo trutta Linnaeus, 1758 and Oncorhynchus mykiss (Walbaum, 1792), with spillover to the native Oreochromis mossambicus (Peters, 1852) and straightfin barb, Enteromius (Barbus) paludinosus (Peters, 1852) also recorded (Basson, 1982; Van As et al., 1984; Bragg, 1991). During a pilot study on the health status of ornamental freshwater fishes imported to South Africa, Mouton et al. (2001) recorded I. multifiliis from guppies, Poecilia reticulata Peters, 1859 and goldfish, Carassius auratus (Linnaeus, 1758). This study clearly demonstrated the potential for continual introductions of this pathogenic parasite through the ornamental fish trade and further emphasised the need for proper health screening of all imported fishes into South Africa. 2.1.2. Apiosoma piscicola Apiosoma piscicola, first described more than 120 years ago from C. carpio collected in France, is a sessile peritrich from the Epistylididae that lives on the gills and body surface of its host (Li et al., 2008). With its native host being C. carpio, it is no surprise that this species has a similar global distribution and status as an invasive species, and has been reported as such from, amongst others, Canada (Cone and Odense, 1987), Egypt (El-Tantawy et al., 2013), and Mexico (Aguilar-Aguilar and Islas-Ortega, 2015). The first report of A. piscicola from South Africa was by Viljoen and Van As (1983) from the skin of the southern mouthbrooder, Pseudocrenilabrus philander (Weber, 1897), collected from the Westdene Dam in the Jukskei River (Table 1). In a follow-up study on sessile peritrichs from freshwater fishes in South Africa, Viljoen and Van As (1985) reported A. piscicola from an additional seven hosts collected in more than ten rivers as well as three fisheries stations (Table 1, Fig. 1B). This wide distribution and host range clearly indicated that this species has been a well-established co-invader long before its first report in the 1980s. As the focus of the Viljoen and Van As (1985) study was the northern regions of South Africa (Gauteng, Limpopo, North West and Mpumalanga provinces), it would be important to determine the presence, distribution and hosts of this alien in the rest of South Africa's rivers. 2.1.3. Chilodonella hexasticha Members of the chilodonelid genus Chilodonella Strand, 1928 that parasitise fishes are known to cause the disease chilodonellosis, which can lead to extreme high host mortalities, especially dua et al., under aquaculture conditions (Mitra and Haldar, 2004; Pa

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7

Fig. 1. Maps indicating the South African distribution records for (A) Ichthyophthirius multifiliis Fouquet, 1876; (B) Apiosoma piscicola (Blanchard, 1885); (C) Chilodonella hexasticha (Kiernik, 1909) and Chilodonella piscicola (Zacharias, 1894); (D) Schyzocotyle (Bothriocephalus) acheilognathi (Yamaguti, 1934).

2013; Bastos Gomes et al., 2017). Two species, C. hexasticha and C. piscicola (Zacharias, 1894) are considered to be the main agents of chilodonellosis and occur globally on the body surface, gills, and fins of freshwater fish hosts. Although the majority of records of pathology caused by Chilodonella spp. are from aquaculture facil€ki et al., 1994), these paraities, such as those in Finland (Rintama sites have also been reported as the main cause of deaths of native fish in natural habitats, such as the Finke River near Alice Springs, Australia (Langdon et al., 1985). In the latter case, Langdon et al. (1985) reported that C. hexasticha induced severe generalised epithelial hyperplasia in the gills, which possibly compromised respiratory exchange and killed the fish through hypoxaemia. The first record of C. hexasticha in South Africa, according to Paperna and Van As (1983), was most probably a conference contribution by Du Plessis (1952). This publication reported mass mortalities of the native Mozambique tilapia, Oreochromis mossambicus, due to heavy infections of a Chilodonella sp., from various fish ponds in South Africa. Its presence in South Africa, and the pathology it caused on native wild caught and farmed fishes, was confirmed by Paperna and Van As (1983) and Van As et al. (1984). Thus far, C. hexasticha has been reported from four cichlids and one

cyprinid collected in more than five river systems and two aquaculture facilities (Table 1, Fig. 1C). No research in South Africa has been conducted on this important pathogen since the 1980s and specifically not regarding the control thereof. Therefore, in the light of the current global and South African drive towards increasing fresh water aquaculture, it is imperative that research into this and other disease causing invasive parasites are prioritised (Bastos Gomes et al., 2017).

2.1.4. Chilodonella piscicola (syn. C. cyprini) The taxonomic status of this Chilodonella species was only resolved in the 1970s when C. cyprini was synonymised with C. piscicola and clear evidence was provided that C. hexasticha and C. piscicola are distinct species (Mitra and Haldar, 2004; Bastos Gomes et al., 2017). It is therefore no surprise that the first records of C. piscicola in South Africa, noted by Basson (1982) and Van As and Basson (1984), initially referred to this species as C. cyprini. These records from South Africa were not included in the recent review of the Chilodonella by Bastos Gomes et al. (2017), most probably due to the original identification as C. cyprini; however, it can now be included with the other seven countries listed as

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confirmed records of C. piscicola. In addition, its presence on two wild caught cichlids, Coptodon rendalli (Boulenger, 1896) and Pseudocrenilabrus philander, is together with the record from Tibet (see Bastos Gomes et al., 2017), the only records of this parasite on native wild caught fishes (Table 1, Fig. 1C). Similar to C. hexasticha, C. piscicola has also been found to cause mortalities in fish aquaculture, however, the former is associated with warmer climates (between 26 and 31  C), while the latter exhibits a wide thermal tolerance in the lower range (between 4 and 20  C) (reviewed by Bastos Gomes et al., 2017). With the majority of South Africa's river and impoundment temperatures dropping down to below 20  C in winter, the potential for C. piscicola to proliferate under these conditions in the wild needs to be investigated. 2.2. Phylum Platyhelminthes 2.2.1. Schyzocotyle (Bothriocephalus) acheilognathi It has been well documented that the Asian tapeworm, S. acheilognathi, was most likely first introduced during 1975 into South Africa with its native host, the grass carp Ctenopharyngodon idella Valenciennes, 1844 (Boomker et al., 1980; Bertasso and Avenant-Oldewage, 2005; Stadtlander et al., 2011). Following its introduction, it successfully established itself in the common carp, Cyprinus carpio (introduced for commercial carp farming). The first published report of this invasive parasite was thus in C. carpio by Boomker et al. (1980), from a commercial fish farm in the Komatipoort area, Mpumalanga Province of South Africa (Table 1, Fig. 1D). As S. acheilognathi appears to not be host specific both on an intermediate or definitive host level, this parasite quickly spilled over to native hosts across South Africa when C. carpio was introduced for aquaculture and recreational angling purposes and C. idella for controlling aquatic weeds (Stadtlander et al., 2011; Ellender and Weyl, 2014). The first record of this species as a co-invader following spillover was that of Brandt et al. (1981) reporting it parasitising the Vaal-Orange largemouth yellowfish, Labeobarbus kimberleyensis Gilchrist and Thompson, 1913, collected from the Vaal Dam in the Vaal River (Fig. 1D). In the same year, Van As et al. (1981) reported another spillover event, this time in Boskop Dam, Mooi River, with the three-spot barb, Enteromius (Barbus) trimaculatus, as the infected host (Fig. 1D). Since these first reports, S. acheilognathi has been reported from at least 10 native hosts (Table 1) from six rivers (Fig. 1D) in South Africa (Mashego, 1982; Barkhuizen, 1991; Schramm, 1992; Retief et al., 2007; Stadtlander et al., 2011; Kuchta et al., 2012; Swanepoel, 2015), making it one of the most widespread co-invasive parasites reported in South Africa. The pathological effects of S. acheilognathi on native hosts in aquaculture conditions, as well as its threat to wild populations, have been well documented globally (Dove et al., 1997; Salgadopez, 2003; Pullen et al., 2009). HowevMaldonado and Pineda-Lo er, research in South Africa has mainly focussed on its distribution, ecology, and potential use as bioindicators of metal pollution (Bertasso and Avenant-Oldewage, 2005; Retief et al., 2007; Degger and Avenant-Oldewage, 2009), with a paucity of data on its population and community level impact on threatened native species. Future studies should specifically focus on these impacts and on regions of high endemicity, such as the Cape Floristic Region of the southern and southwestern Cape Province where the largest percentage of South Africa's threatened freshwater fishes occur. 2.3. Phylum Arthropoda 2.3.1. Lernaea cyprinacea The global distribution of the copepod Lernaea cyprinacea as an invasive ectoparasite, and the severe effects of it on native

freshwater fish hosts, has been well documented (see Welicky et al., 2017). Despite the first record of the introduction of this ectoparasite into Africa dating back to the 1960s (Robinson and AvenantOldewage, 1996), it was only recorded for the first time from South Africa twenty years later. Van As and Basson (1984) recognise the unpublished Masters dissertation of Viljoen (1982) as the first document to report L. cyprinacea from South Africa. In addition to Viljoen (1982) records of O. mossambicus and Labeobarbus marequensis (Smith, 1841) from Hartebeespoort Dam in the Crocodile River (West) and Labeo cylindricus Peters, 1852 from the Limpopo River as hosts, Van As and Basson (1984) recorded an infestation of L. cyprinacea on O. mossambicus from the Lowveld Fisheries Station (Table 1, Fig. 2A). Further confirmation of the presence of L. cyprinacea on South African native fishes was by Van As and Viljoen (1984) and Viljoen (1986) who also reported the presence of L. cyprinacea on O. mossambicus in Hartebeespoort Dam as well as from Labeo congoro Peters, 1852 (syn. Labeo rubropunctatus) in the Glen Alpine Dam, Mogalakwena River (Table 1, Fig. 2A). Interestingly, Bruton and Merron (1985) included L. cyprinacea in their list of what they considered to be doubtful alien species and therefore De Moor and Bruton (1988) did not include this species in their atlas to alien aquatic animals in southern Africa. More than ten years later Robinson and Avenant-Oldewage (1996) increased our knowledge on the distribution and hosts of L. cyprinacea and added another six cyprinid hosts collected from three different rivers (Table 1, Fig. 2A). These authors also provided a detailed morphological study of L. cyprinacea as well as an updated geographical distribution in Africa. Recently the identity of L. cyprinacea in South Africa was genetically confirmed and two more hosts and three localities where added (Smit et al., 2016; Truter et al., 2016; Welicky et al., 2017). The most surprising fact regarding the host records of L. cyprinacea in South Africa is that it does not include any of the invasive cyprinids which were potentially responsible for the co-introduction and subsequent coinvasion of this parasite. Globally, the severe effects on native freshwater fish hosts by L. cyprinacea have been well documented; however, the first study on the impact of this co-invader on native fish health in South Africa is the recent work by Welicky et al. (2017). In their paper, the authors reported on the change in host health following a natural drought induced treatment for L. cyprinacea, leaving hosts without this parasite in a much better overall health state than those infected. Future work should include host immune response to infection as well as laboratory based studies on the effect of L. cyprinacea on host fitness. 2.3.2. Argulus japonicus With a very low host specificity, and one of its hosts from its native range (C. carpio) being considered among 100 of the world's worst invasive alien species (Lowe et al., 2000), it is no surprise that the Japanese fish louse, A. japonicus, is one of the most prevalent and widespread co-invaders in South African freshwater systems. Although reports exist that C. carpio, and its other native host, the goldfish Carassius auratus, were already introduced into South Africa in 1859 and 1726 respectively (De Moor and Bruton, 1988), the first official record of the co-invading A. japonicus was only in 1983. Kruger et al. (1983) reported it from 11 hosts, including C. carpio, from two sites (Lake Baberspan and Bloemhof Dam) in the OrangeVaal River system (Table 1, Fig. 2B). However, it was clear that the introduction of A. japonicus happened much earlier, with Van As and Basson (1984) adding another five hosts and four more localities, including sites from the Crocodile River (West) (Hartbeespoort Dam and Roodeplaat Dam), showing a wide spread occurrence not typically associated with a recent introduction. Van As (1987) supported this and went further by proposing that the records of Argulus spp. by Du Plessis (1952) and Lombard (1968)

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from the South African Mpumalanga Province were in fact A. japonicus, indicating a much earlier introduction. Following the above reports, additional records of its co-invasion have been published, clearly indicating its wide distribution throughout South Africa (Fig. 2B) and successful spillover onto at least nine native hosts (Avenant-Oldewage, 1994, 2001). Although more recent work on A. japonicus in South Africa focussed on its anatomy, ultrastructure, and reproduction (Tam and Avenant-Oldewage, 2006; Avenant-Oldewage and Everts, 2010), there are still gaps in our knowledge on the full extent of its distribution throughout South Africa and its impact on native fishes at population and community levels. 3. Confirmed co-introduced freshwater fish parasites 3.1. Phylum Euglenozoa 3.1.1. Ichthyobodo necator The ectoparasitic flagellate I. necator has been implicated in disease and mortality of cultured fish globally and is, amongst other things, probably the major cause of death of cultured salmonid fry

9

in Scottish fish farms (Robertson, 1985). In South Africa, specimens identified as I. necator have been reported in the early 1980s from three native cyprinids and the alien C. carpio. These specimens were collected from impoundments in two rivers in the Limpopo Province (Paperna and Van As, 1983; Van As and Basson, 1984), and an aquaculture facility and a river (Kouga River) in the Eastern Cape Province of South Africa (Van As and Basson, 1984) (Fig. 2C). More recently, Ichthyobodo Pinto, 1928 isolates collected from pondreared koi-carp C. carpio fry from South Africa (specific locality not known) were included in a molecular study by Todal et al. (2004) that aimed to test previous suggestions that I. necator comprises a complex of species. Todal et al. (2004) concluded that there were at least eight strains or species from the 14 isolates tested. The South African isolate showed the highest sequence similarity with the isolate from C. auratus collected in Singapore and grouped together with isolates from an Apistogramma sp. (Brazil) and a Morone Mitchill, 1814 hybrid (USA) (Todal et al., 2004). This molecular evidence suggests that the Ichthyobodo isolate from C. carpio in South Africa can be considered as cointroduced. However, the I. necator identified from native fishes needs to be molecular characterised in order to determine whether

Fig. 2. Maps indicating the South African distribution records for (A) Lernaea cyprinacea Linnaeus, 1758; (B) Argulus japonicus Thiele, 1900; (C) Ichthyobodo necator Henneguy, 1883 (needs molecular confirmation); (D) Trichodina acuta Lom, 1961, Trichodina mutabilis Kazubski and Migala, 1968, Trichodina reticulata Hirschmann and Partsch, 1955, and Trichodina uniforma Van As and Basson, 1989.

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they are co-invaders spilled over from C. carpio or are a native South African sibling species.

3.2. Phylum Ciliophora 3.2.1. Trichodina acuta The mobilid peritrich, T. acuta, is a known invasive parasite and has, since its original description, been reported from at least seven different non-native regions (Basson and Van As, 1993). In South Africa, Basson et al. (1983) reported T. acuta from four cichlids and two cyprinid species collected at more than six different localities in the northern provinces of South Africa. These hosts included T. acuta's type host, C. carpio, and thus further strengthened their conclusion that this parasite is a co-introduced species that spilled over to South African native fishes. However, in their remarks on the species, Basson et al. (1983) commented on the distinct variability in size and denticle dimensions between the South African population and those reported from Israel and the Philippines. Van As et al. (1984) also reported what they identified as T. acuta from a Fisheries Research Station where it was implicated in the mortalities of two different fish species. Bruton and Merron (1985) and De Moor and Bruton (1988) further included this species in their respective lists of confirmed invasive aquatic invertebrates. In their review on the taxonomic status of fish ectoparasitic trichodinids, Van As and Basson (1989), with new information available to them, re-evaluated their original records of T. acuta from South Africa. By using additional characteristics which enabled them to provide a better understanding of differences in denticle shape, Van As and Basson (1989) described what was previously identified as a South African population of T. acuta, as all belonging to a new species, Trichodina compacta Van As and Basson, 1989, thereby removing T. acuta from the list of invasive parasites from South Africa. However, a few years later, Basson and Van As (1993) accurately identified T. acuta in South Africa and this time on rainbow trout, Oncorhynchus mykiss (Walbaum, 1792). This species was collected from a cage culture on a trout farm in the Free State province of South Africa (Table 1, Fig. 2D) confirming its status as a co-introduced parasite in South Africa. Basson and Van As (1993) also provided a detailed discussion on possible routes of introduction into South Africa, especially since its native hosts are European and Asian cyprinids and not salmonids, and concluded that it must have been a recent introduction and future research should focus on the potential spillover to South African native hosts.

3.2.2. Trichodina mutabilis The history of discovery of T. mutabilis from South Africa is similar to that of T. acuta (see above) and thus not repeated here in detail. In short, Basson et al. (1983) reported this species from various invasive and native hosts in South Africa and then later Van As and Basson (1989) redescribed those specimens thought to be T. mutabilis as two species new to science, Trichodina kazubskii Van As and Basson, 1989 parasitising native fishes and Trichodina uniforma Van As and Basson, 1989 from the introduced C. auratus (see section 3.2.4). More than ten years later, Mouton et al. (2001) reported T. mutabilis again from South Africa, describing this parasite from C. carassius during a health survey of ornamental fishes imported to South Africa (Table 1, Fig. 2D). The fact that spillover of T. mutabilis to native non-cyprinid hosts in India (Mitra and Bandyopadhyay, 2005), and its heavy infection on moribund C. carpio in an aquaculture facility in the USA (Kritsky and Heckmann, 2002) has been reported, shows the potential threat of this co-introduced parasite to both native species and aquaculture in South Africa.

3.2.3. Trichodina reticulata As one of the most prevalent ectoparasites of the goldfish, C. auratus, it is not surprising that T. reticulata has a similar global distribution to that of its popular ornamental fish host. Basson and Van As (1993) found this to be true when they recorded T. reticulata from C. auratus obtained from a local ornamental fish distributor in Bloemfontein, South Africa (Table 1, Fig. 2D). Notwithstanding being reported from more than 12 countries (Martins et al., 2012), it has never been implicated in spillover to native hosts. This is confirmed by the study of Dove and O'Donoghue (2005) who examined 2003 fishes belonging to 33 species from 58 sites in Queensland, Australia, and only found T. reticulata on wild caught C. auratus and another introduced species, the Eastern mosquitofish Gambusia holbrooki Girard, 1859. Based on current available information, it is most likely that if T. reticulata does get into South Africa's natural waterways it will remain a co-introduced parasite with a low possibility of spillover, however this needs to be further investigated. 3.2.4. Trichodina uniforma As mentioned above (section 3.2.2), T. uniforma described by Van As and Basson (1989) from C. auratus was originally identified as the invasive T. mutabilis. The same authors further concluded that despite extensive surveys throughout southern Africa, they did not find this species in any other locality other than the original fish farm in the Komatipoort River, which they described it from, nor on any other hosts other than the introduced C. auratus (Table 1, Fig. 2D). This raised the question as to whether T. uniforma was cointroduced with C. auratus or if it was spillback from its native hosts. Since its description in 1989, various authors have reported this species from (amongst other hosts) C. auratus and C. carpio from their native range in China (see Tang et al., 2007; Qi et al., 2011; Li et al., 2014), thus confirming its status as a co-introduced parasite in South Africa. Recently, Tang and Zhao (2016), using 18S rDNA, supported Van As and Basson (1989) morphological identification of T. uniforma as a separate species to T. mutabilis. 3.3. Phylum Platyhelminthes 3.3.1. Atractolytocestus huronensis One of the most recent reports of a co-introduced parasite from South Africa is that of the cestode A. huronensi. Scholz et al. (2015) reported this tapeworm from the intestine of C. carpio from four localities in the Limpopo Province of South Africa (Table 1, Fig. 3B). Their paper was also the first to include morphological and molecular confirmation of the identity of the introduced parasite. Although Scholz et al.'s (2015) report on this co-introduction is recent, the co-introduction of A. huronensi into South Africa might not be. During parasitological surveys conducted between 2013 and 2016 by the authors of this review in the Vaal River (North West Province), as well as in the Riet River (Northern Cape Province), A. huronensi specimens were collected from C. carpio at both sites (Smit unpublished records). These records are now included here (Table 1, Fig. 3A) and demonstrate a much wider distribution in different river systems than originally thought, and thus an unlikely pattern usually seen in a recent introduction. We concur with Scholz et al. (2015) that future work on this tapeworm should include phylogeographic studies employing molecular markers to reveal the source of introduction of this co-introduced parasite. 3.3.2. Acolpenteron ureteroecetes The first record of a co-introduced parasite into South Africa is, according to our records, that of Du Plessis (1948), who reported the presence of the monogenean A. ureteroecetes in the urethras of de, 1802), three bass species, Micropterus dolomieu (Lacepe

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Micropterus punctulatus (Rafinesque, 1819), and Micropterus salde, 1802), bred in the Jonkershoek Fish Hatchery, moides (Lacepe Western Cape Province. Although all three species were infected, only M. salmoides had high parasite loads that directly lead to the mortality of large numbers of fingerlings (Du Plessis, 1948). Mortality of cultured M. salmoides due to A. ureteroecetes infections were more recently reported by Petrie-Hanson (2001) from pond reared fish in Mississippi, USA, confirming Du Plessis' (1948) original observation of A. ureteroecetes' pathogenicity. The only record of A. ureteroecetes in wild M. salmoides from South Africa is a nonpeer reviewed published conference abstract by Matla et al. (2010) reporting a very low infection of this species from the ureterurinary bladder of M. salmoides collected in the Tzaneen Dam, Limpopo Province (Table 1, Fig. 3B). As the stocking of most of the M. salmoides populations in South Africa was via the Jonkershoek Fish Hatchery (De Moor and Bruton, 1988), the co-introduction of A. ureteroecetes into the Limpopo Province was most likely from the original Jonkershoek Fish Hatchery stock. Research into the parasites of other populations of M. salmoides will most probably reveal a much wider distribution of A. ureteroecetes in South Africa and warrants further research.

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3.3.3. Dactylogyrus extensus, Dactylogyrus minutus and Dactylogyrus lamellatus The three dactylogyrids, D. extensus, D. minutus, and D. lamellatus are well documented known co-invaders, with their widely introduced host, C. carpio, for the former two and the grass carp, Ctenopharyngodon idella for the latter (Dove and Ernst, 1998; Yang et al., 2016). Crafford et al. (2014a) recorded all three of these species from their respective wild caught introduced hosts from the Vaal Dam in the Vaal River, South Africa (Table 1, Fig. 3C), with Dactylogyrus extensus and D. minutus collected from C. carpio, and D lamellatus from C. idella. With representatives of Dactylogyrus Diesing, 1850 considered to be very host specific, the chances of host switching to native fish by these co-invaders are limited (Dove  et al., 2001). This is further supported by and Ernst, 1998; Simkova the work of Crafford et al. (2012; 2014a,b) on the monegeneans of fishes from the Vaal Dam, who did not report any spillover of these introduced Dactylogyrus species onto any of the native hosts studied. 3.3.4. Gyrodactylus kherulensis The gyrodactylid G. kherulensis is a parasite of the common as well as the koi carp, C. carpio koi. Similar to the dactylogyrids

Fig. 3. Maps indicating the South African distribution records for (A) Atractolytocestus huronensis Anthony, 1958; (B) Acolpenteron ureteroecetes Fischthal and Allison, 1940; (C) Dactylogyrus extensus Mueller and Van Cleave, 1932, Dactylogyrus minutus Kulwiec, 1927 and Dactylogyrus lamellatus Achmerow, 1952; (D) Gyrodactylus kherulensis Ergens, 1974.

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reported above, G. kherulensis has also been co-introduced worldwide due to the popularity of its natural host as an aquaculture and ornamental species. The first report of G. kherulensis in South Africa was in a non-peer reviewed published conference abstract by Maseng et al. (2010). These authors collected G. kherulensis from commercially bought, as well as wild caught, C. carpio in the Western Cape Province of South Africa (Table 1, Fig. 3D). Recently Crafford et al. (2014a) found a total of three G. kherulensis specimens on the body surface of a single C. carpio, collected from the Vaal Dam in the Vaal River (Table 1, Fig. 3D), confirming its status as a co-introduced parasite in South Africa.

introduced with its ornamental fish hosts. In a non-peer reviewed published conference abstract by Maseng et al. (2010), the authors reported G. kobayashii present on both commercially bought, as well as wild caught, C. auratus in the Western Cape Province of South Africa (Table 1). Maseng et al. (2010) did not list the specific locality of the wild caught fish in the conference abstract but indicated the locality as the Kuils River in her unpublished Masters dissertation (Maseng, 2010). As this record of the cointroduction of G. kobayashii into South Africa is in non-peer reviewed publications, these records are classified as uncertain until formal publication thereof.

3.3.5. Ancyrocephalid monogeneans of largemouth bass, Micropterus salmoides As part of this special issue on invasive parasites, Truter et al. (2017) provided the first peer reviewed published record of five ancyrocephalid monogeneans form largemouth bass, Micropterus salmoides, collected at three localities in South Africa. In that paper the authors provide full descriptions as well as distribution records and maps (see Truter et al., 2017), for these species. For completeness of the current review these species, Clavunculus bursatus (Mueller, 1963), Onchocleidus dispar (Mueller, 1936), O. furcatus (Mueller, 1937), O. principalis (Mizelle, 1936) and Syncleithrium fusiformis (Mueller, 1934) are only listed here and not further discussed.

4.2.2. Pseudodactylogyrus anguillae The monogenean, P. anguillae, is an ectoparasite originally described from the gills of the Japanese eel, Anguilla japonica Temminck and Schlegel, 1846. Following its original description, it was discovered to have invaded Europe where it was first found in 1977 on the gills of the European eel, Anguilla anguilla from an eel farm in the western Soviet Union (Buchmann et al., 1987). Pseudodactylogyrus anguillae has subsequently been recorded from wild populations of the American eel, Anguilla rostrata (Lesueur, 1817) in Canada (Cone and Marcogliese, 1995) and the USA (Hayward et al., 2001). The first report from South Africa was by Christison and Baker (2007) who reported P. anguillae from the gills of the longfin eel, Anguilla mossambica collected from four rivers in the Eastern Cape (Table 1). Parker et al. (2011) and McHugh et al. (2017) subsequently extended the distribution range by including additional sites from the Eastern Cape (Table 1). However, Ogawa et al. (2015) and McHugh et al. (2017) raised concerns about the identity of what was thought to be P. anguillae from South Africa as its origin in this region is uncertain since no record of the introduction of A. japonica, or any other non-native eels into South Africa, can be found (Ellender and Weyl, 2014). Until further molecular analysis on the South African population of P. anguillae, using a combination of different genetic markers, has been completed and its identity confirmed, we provisionally assign this species to the uncertain invasive status category.

4. Parasites of uncertain invasive status 4.1. Phylum Ciliophora 4.1.1. Apiosoma nasalis This sessile peritrich was originally described from the nasal cavities of cyprinids from the Amur River Basin, Russia; however, in his taxonomic revision of this genus, Lom (1966) suggested that reexamination of live specimens of this species is needed to confirm its identity. Its possible presence in South Africa was first recorded by Viljoen and Van As (1983) from Pseudocrenilabrus philander collected in the Westdene Dam, Johannesburg (Table 1). The authors acknowledged the uncertainty regarding its identity, especially as they collected it from the skin and gills and not the nasal cavities, and therefore proposed that their identification be provisional until more material from other localities and fish species are collected. However, in Viljoen and Van As (1985) the same authors recorded A. nasalis from P. philander, again from the Westdene Dam, but this time without stating any uncertainties. It is thus not clear if the 1985 record was from new material or just a repeat of the 1983 record. As the 1985 record did not include more fish hosts from different localities as proposed by Viljoen and Van As (1983), the invasive status of this species is considered as uncertain. 4.1.2. Trichodinella epizootica and Trichodina nigra Both T. epizootica and T. nigra were included in the report by Basson et al. (1983) on trichodinids from selected fishes of South Africa (also see section 3.2.1.). Basson and Van As (1993), however, suspected that their original identification was incorrect and that re-evaluation of these species will most likely show that they are not representatives of either T. epizootica or T. nigra. Until proper reevaluation, we place both these species here in the uncertain invasion status category.

4.3. Phylum Arthropoda 4.3.1. Achtheres pimelodi (syn. Achtheres micropteri) The lernaeopodid copepod, A. pimelodi, is an ectoparasite found on the gills of various fish host in the USA, including the smallmouth bass, M. dolomieu (Muzzall and Whelan, 2011). Barnard (1955) presumed that A. pimelodi (using the synonym A. micropteri) might have been introduced into South Africa with the smallmouth bass, M. dolomieu, but it is not clear whether he actually collected any from South Africa. Later, Fryer (1968) listed this species (also using the synonym A. micropteri) in his paper on the distribution of parasitic Crustacea from African freshwater fish, but once again there was no indication on whether he collected any himself or if he was just referencing Barnard (1955). No other record of this parasite from South Africa exists and thus its current status as alien in South African waters is doubtful and needs further study. 5. Species previously reported as invasive but hereby removed from the list 5.1. Phylum Ciliophora

4.2. Phylum Platyhelminthes 4.2.1. Gyrodactylus kobayashii The gyrodactylid, G. kobayashii, is a parasite of the goldfish, C. auratus, and has a world-wide distribution due to it being co-

5.1.1. Trichodina pediculus Basson et al. (1983) originally reported Trichodina pediculus Ehrenberg, 1838 from two cichlids in South Africa, but later Van As and Basson (1989) corrected the original identification and

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Table 2 Fish hosts with known alien parasites from South Africa. Classification

Genus species

Parasite species

Family: Mormyridae

Marcusenius macrolepidotus

Apiosoma piscicola

Family: Anguillidae

Anguilla mossambica

Ichthyophthirius multifiliis

Family: Cyprinidae

Carassius auratus

Ichthyophthirius multifiliis Trichodina mutabilis Trichodina reticulata Trichodina uniforma Argulus japonicus Atractolytocestus huronensis Dactylogyrus minutus Dactylogyrus lamellatus Gyrodactylus kherulensis Ichthyophthirius multifiliis Ichthyobodo necator Schyzocotyle acheilognathi Schyzocotyle acheilognathi Schyzocotyle acheilognathi Schyzocotyle acheilognathi Apiosoma piscicola Schyzocotyle acheilognathi Schyzocotyle acheilognathi Apiosoma piscicola Chilodonella hexasticha Ichthyophthirius multifiliis Schyzocotyle acheilognathi Argulus japonicus Schyzocotyle acheilognathi Argulus japonicus Lernaea cyprinacea Schyzocotyle acheilognathi Argulus japonicus Schyzocotyle acheilognathi Argulus japonicus Lernaea cyprinacea Lernaea cyprinacea Schyzocotyle acheilognathi Argulus japonicus Lernaea cyprinacea Argulus japonicus Lernaea cyprinacea Argulus japonicus Lernaea cyprinacea Lernaea cyprinacea Lernaea cyprinacea Lernaea cyprinacea

Cyprinus carpio

Enteromius Enteromius Enteromius Enteromius

annectens brevipinnis bifrenatus trimaculatus

Enteromius argenteus Enteromius paludinosus

Enteromius mattozi Labeobarbus kimberleyensis

Labeobarbus aeneus Labeobarbus marequensis

Labeo umbratus Labeo capensis Labeo rosae Labeo ruddi Labeo congoro Labeo cylindricus Family: Clariidae

Clarias gariepinus

Argulus japonicus Dactylogyrus extensus

Family: Salmonidae

Salmo trutta Oncorhynchus mykiss

Ichthyophthirius multifiliis Argulus japonicus Ichthyophthirius multifiliis Trichodina acuta

Family: Centrarchidae

Micropterus salmoides

Acolpenteron ureteroecetes Clavunculus bursatus Onchocleidus dispar Onchocleidus furcatus Onchocleidus principalis Syncleithrium fusiformis Apiosoma piscicola Acolpenteron ureteroecetes Acolpenteron ureteroecetes

Micropterus dolomieu Micropterus punctulatus Family: Cichlidae

Pseudocrenilabrus philander

Tilapia sparrmanii

Coptodon rendallii

Apiosoma piscicola Chilodonella piscicola (syn C. cyprini) Chilodonella hexasticha Ichthyobodo necator Lernaea cyprinacea Ichthyobodo necator Chilodonella piscicola (syn C. cyprini) Chilodonella hexasticha Apiosoma piscicola Chilodonella piscicola (syn C. cyprini) Chilodonella hexasticha Lernaea cyprinacea (continued on next page)

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N.J. Smit et al. / International Journal for Parasitology: Parasites and Wildlife xxx (2017) 1e16 Table 2 (continued ) Classification

Family: Poeciliidae

Genus species

Parasite species

Oreochromis mossambicus

Apiosoma piscicola Argulus japonicus Chilodonella piscicola (syn C. cyprini) Chilodonella hexasticha Ichthyobodo necator Ichthyophthirius multifiliis Lernaea cyprinacea

Poecilia reticulata

Ichthyophthirius multifiliis

described the original specimens as Trichodina magna Van As and Basson, 1989. This correction was confirmed by Basson and Van As (1993), and as no further reports of T. pediculus from South Africa exists, it is hereby removed from the list of invasive freshwater fish parasites of South Africa. 6. Conclusions and future direction All previously reported alien freshwater fish parasites were reviewed and categorised according to their invasive status. Based on available information, seven species were classified as coinvasive, 16 as co-introduced, six as uncertain invasive status, and a single species previously reported as invasive was removed from the list. The total confirmed number of alien parasites (23) in South Africa is low when considering that at least 17 species of alien freshwater fishes are established in South African waters, with the majority of the first introductions dating back to the mid twentieth century (Ellender and Weyl, 2014). Possible reasons for the low numbers of alien parasites might include that the original introductions where from stock already low in parasite diversity, for example, largemouth bass were introduced into South Africa from breeding facilities in Europe (De Moor and Bruton, 1988); or that the South African environment, although suitable to the host, is not suitable for its parasites. However, the most likely reason is probably the lack of extensive parasitological surveys in all the different regions of South Africa, as the current distribution records of alien parasites in South Africa is more related to the distribution of fish parasitologists than that of the parasites themself [see Van As (2015) and Smit and Hadfield (2015) for reviews on the history of fish parasitology in South Africa]. A more targeted approached focussing specifically on South Africa's coastal provinces should provide more accurate information on the current distribution and diversity of invasive freshwater fish parasites. The role of invasive parasites in mass fish-kill events in natural systems has already been established, for example, in Australia Langdon et al. (1985) identified invasive Chilodonella spp. as the main cause of death of native fish in the Finke River near Alice Springs (also see section 2.1.3.). In South Africa, mass fish-kill events are often reported and usually attributed to sudden change in water temperature, oxygen levels, and stressors such as pollution, and potentially even invasive fishes (Wepener et al., 2011), however, thus far invasive parasites have not been considered as a contributing factor or even the cause of these incidents. Future research on invasive parasites in South Africa should therefore include their potential role in mass fish-kill events. To date, no research in South Africa (and very limited internationally) has focussed on the co-introduction of parasites by translocated species, especially those that were introduced through inter-basin water transfer schemes. Ellender and Weyl (2014) listed 21 extralimited fish species that were already established in their new environments. Future research should therefore also focus on the parasites of these species in both their native and introduced

range, as well as the possible spillover to native fishes. One of the biggest challenges when working with invasive parasites is the confirmation of the identity of the species, especially if representatives of the same family or even genus occur naturally in that region. We therefore propose that all future work on invasive parasites should include both morphological and molecular approaches when determining the species. It is also of utmost importance to deposit voucher specimens into recognised collection facilities for future verification, comparison, and research in general. Although this review specifically deals with freshwater fish parasites introduced into South Africa, the information presented on the majority of the different parasites is also applicable to the rest of Africa and other countries worldwide. Similarly, the need for future research on the role of invasive parasites in fish-kills, parasites introduced by extralimited fishes, as well as the molecular identification and deposition of voucher specimens, should be prioritised globally. Conflict of interest The authors declare there is no conflict of interest. Acknowledgements Research funding from the South African National Research Foundation (NRF) is hereby acknowledged (NRF project IFR170210222411 Grant 109352, NJ Smit, PI). Opinions expressed, and conclusions arrived at, are those of the authors and are not necessarily those of the NRF. Financial assistance for KA Hadfield from the Claude Leon Foundation and the Western Indian Ocean Marine Science Association (WIOMSA) Marine Research Grant for this research is also acknowledged. Dr. Scott Lawton, Kingston s Scholz, Institute of Parasitology, University, UK and Prof Toma Czech Republic are thanked for the identification of the Schyzocotyle acheilognathi collected from the Vaal River and Riet River respectively. This is contribution number 197 of the North-West University (NWU) Water Research Group. References Adlard, R.D., Miller, T.L., Smit, N.J., 2015. The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends Parasitol. 31, 160e166. Aguilar-Aguilar, R., Islas-Ortega, A.G., 2015. A checklist of ciliate parasites (Ciliophora) of fishes from Mexico. Zootaxa 4027, 270e280. Avenant-Oldewage, A., 1994. A new species of Argulus from Kosi Bay, South Africa and distribution records of the genus. Koedoe 37, 89e95. Avenant-Oldewage, A., 2001. Argulus japonicus in the Olifants River system possible conservation threat? S. Afr. J. Wildl. Res. 31, 59e63. Avenant-Oldewage, A., Everts, L., 2010. Argulus japonicus: sperm transfer by means of a spermatophore on Carassius auratus (L). Exp. Parasitol. 126, 232e238. € van die vislintwurm, Bothriocephalus Barkhuizen, L.M., 1991. Lewenstrategiee acheilognathi Yamaguti, 1934 in die Oranje Vrystaat. M.Sc. dissertation. University of the Orange Free State, South Africa, p. 195.

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